Effects of erythropoiesis-stimulating agents on fatigue-and anaemia-related symptoms in cancer patients: Systematic review and meta-analyses of published and unpublished data

British Journal of Cancer

Volumn 111, Issue 1, 2014, Pages 33-45

  Bohlius, J ^a   Tonia, T ^a   Nuesch E ^a,b   Juni P ^a   Fey, M F ^c   Egger, M ^a   Bernhard, J ^c  

^a UNIVERSITY OF BERN   (Switzerland)

^b LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

erythropoiesis stimulating agents; meta analysis; quality of life

Indexed keywords

ANTIANEMIC AGENT; HEMOGLOBIN; NOVEL ERYTHROPOIESIS STIMULATING PROTEIN; RECOMBINANT ERYTHROPOIETIN;

ANEMIA; CANCER CHEMOTHERAPY; CANCER FATIGUE; CANCER PATIENT; DRUG EFFECT; FUNCTIONAL ASSESSMENT OF CANCER THERAPY ANEMIA SCALE; FUNCTIONAL ASSESSMENT OF CANCER THERAPY FATIGUE SCALE; HEMOGLOBIN BLOOD LEVEL; HUMAN; META ANALYSIS; PRIORITY JOURNAL; QUALITY OF LIFE; RANDOMIZED CONTROLLED TRIAL (TOPIC); RATING SCALE; REVIEW; SYMPTOMATOLOGY; SYSTEMATIC REVIEW; TREATMENT OUTCOME;

ANEMIA; ERYTHROPOIESIS; FATIGUE; HEMATINICS; HUMANS; NEOPLASMS; QUALITY OF LIFE; RANDOMIZED CONTROLLED TRIALS AS TOPIC; TREATMENT OUTCOME;

EID: 84904131349     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2014.171     Document Type: Review

References (111)

1. Aapro M, Jelkmann W, Constantinescu SN, Leyland-Jones B (2012) Effects of erythropoietin receptors and erythropoiesis-stimulating agents on disease progression in cancer. Br J Cancer 106(7): 1249-1258.
2. Aapro M, Leonard RC, Barnadas A, Marangolo M, Untch M, Malamos N, Mayordomo J, Reichert D, Pedrini JL, Ukarma L, Scherhag A, Burger HU (2008a) Effect of once-weekly epoetin beta on survival in patients with metastatic breast cancer receiving anthracycline-and/or taxane-based chemotherapy: Results of the Breast Cancer-Anemia and the Value of Erythropoietin (BRAVE) study. J Clin Oncol 26(4): 592-598.
3. Aapro M, Osterwalder B, Scherhag A, Burger HU (2009) Epoetin-beta treatment in patients with cancer chemotherapy-induced anaemia: The impact of initial haemoglobin and target haemoglobin levels on survival, tumour progression and thromboembolic events. Br J Cancer 101(12): 1961-1971.
4. Aapro M, Scherhag A, Burger HU (2008b) Effect of treatment with epoetin-beta on survival, tumour progression and thromboembolic events in patients with cancer: An updated meta-analysis of 12 randomised controlled studies including 2301 patients. Br J Cancer 99(1): 14-22.
5. Aapro MS, Link H (2008) September 2007 update on EORTC guidelines and anemia management with erythropoiesis-stimulating agents. Oncologist 13(Suppl 3): 33-36.
6. Aaronson NK, Ahmedzai S, Bergman B, Bullinger M, Cull A, Duez NJ, Filiberti A, Flechtner H, Fleishman SB, de Haes JC (1993) The European Organization for Research and Treatment of Cancer QLQ-C30: A quality-of-life instrument for use in international clinical trials in oncology. J Natl Cancer Inst 85(5): 365-376.
7. Abels R (1993) Erythropoietin for anaemia in cancer patients. Eur J Cancer 29A(Suppl 2): S2-S8.
8. AGO-OVAR 2.7. Reinduction Chemotherapy Containing Carboplatin and Paclitaxel With or Without Epoetin Alpha in Recurrent Platinum Sensitive Ovarian Cancer, Cancer of the Fallopian Tube or Peritoneum. Study terminated and unpublished (ClinicalTrials.gov Identifier: NCT00189371).
9. Arcasoy MO, Amin K, Chou SC, Haroon ZA, Varia M, Raleigh JA (2005) Erythropoietin and erythropoietin receptor expression in head and neck cancer: Relationship to tumor hypoxia. Clin Cancer Res 11(1): 20-27.
10. Bennett CL, Silver SM, Djulbegovic B, Samaras AT, Blau CA, Gleason KJ, Barnato SE, Elverman KM, Courtney DM, McKoy JM, Edwards BJ, Tigue CC, Raisch DW, Yarnold PR, Dorr DA, Kuzel TM, Tallman MS, Trifilio SM, West DP, Lai SY, Henke M (2008) Venous thromboembolism and mortality associated with recombinant erythropoietin and darbepoetin administration for the treatment of cancer-associated anemia. JAMA 299(8): 914-924.
11. Bennett CL, Lai SY, Henke M, Barnato SE, Armitage JO, Sartor O (2010) Association between pharmaceutical support and basic science research on erythropoiesis-stimulating agents. Arch Intern Med 170(16): 1490-1498.
12. Berlin JA, Santanna J, Schmid CH, Szczech LA, Feldman HI (2002) Individual patient-versus group-level data meta-regressions for the investigation of treatment effect modifiers: Ecological bias rears its ugly head. Stat Med 21(3): 371-387.
13. Bohlius J, Schmidlin K, Brillant C, Schwarzer G, Trelle S, Seidenfeld J, Zwahlen M, Clarke M, Weingart O, Kluge S, Piper M, Rades D, Steensma DP, Djulbegovic B, Fey MF, Ray-Coquard I, Machtay M, Moebus V, Thomas G, Untch M, Schumacher M, Egger M, Engert A (2009a) Recombinant human erythropoiesis- stimulating agents and mortality in patients with cancer: A meta-analysis of randomised trials. Lancet 373(9674): 1532-1542.
14. Bohlius J, Schmidlin K, Brillant C, Schwarzer G, Trelle S, Seidenfeld J, Zwahlen M, Clarke MJ, Weingart O, Kluge S, Piper M, Napoli M, Rades D, Steensma D, Djulbegovic B, Fey MF, Ray-Coquard I, Moebus V, Thomas G, Untch M, Schumacher M, Egger M, Engert A (2009b) Erythropoietin or Darbepoetin for patients with cancer-meta-analysis based on individual patient data. Cochrane Database Syst Rev 3: CD007303.
15. Bohlius J, Wilson J, Seidenfeld J, Piper M, Schwarzer G, Sandercock J, Trelle S, Weingart O, Bayliss S, Brunskill S, Djulbegovic B, Benett CL, Langensiepen S, Hyde C, Engert E (2006a) Erythropoietin or darbepoetin for patients with cancer. Cochrane Database Syst Rev 3: CD003407.
16. Bohlius J, Wilson J, Seidenfeld J, Piper M, Schwarzer G, Sandercock J, Trelle S, Weingart O, Bayliss S, Djulbegovic B, Bennett CL, Langensiepen S, Hyde C, Engert A (2006b) Recombinant human erythropoietins and cancer patients: Updated meta-analysis of 57 studies including 9353 patients. J Natl Cancer Inst 98(10): 708-714.
17. Boogaerts M, Coiffier B, Kainz C (2003) Impact of epoetin beta on quality of life in patients with malignant disease. Br J Cancer 88(7): 988-995.
18. Case Jr DC, Bukowski RM, Carey RW, Fishkin EH, Henry DH, Jacobson RJ, Jones SE, Keller AM, Kugler JW, Nichols CR (1993) Recombinant human erythropoietin therapy for anemic cancer patients on combination chemotherapy. J Natl Cancer Inst 85(10): 801-806.
19. Cella D (1997) The Functional Assessment of Cancer Therapy-Anemia (FACT-An) Scale: A new tool for the assessment of outcomes in cancer anemia and fatigue. Semin Hematol 34(3 Suppl 2): 13-19.
20. Cella D (2007) The Functional Assessment of Chronic Illness Therapy-Fatigue (FACIT-F) Scale: Summary of development and validation. FACIT.org: Elmhurst, IL.
21. Cella D, Bullinger M, Scott C, Barofsky I (2002a) Group vs individual approaches to understanding the clinical significance of differences or changes in funnel plot. Mayo Clin Proc 77(4): 384-392.
22. Cella D, Eton DT, Lai JS, Peterman AH, Merkel DE (2002b) Combining anchor and distribution-based methods to derive minimal clinically important differences on the Functional Assessment of Cancer Therapy (FACT) anemia and fatigue scales. J Pain SymptomManage 24(6): 547-561.
23. Cella D, Zagari MJ, Vandoros C, Gagnon DD, Hurtz HJ, Nortier JW (2003) Epoetin alfa treatment results in clinically significant improvements in quality of life in anemic cancer patients when referenced to the general population. J Clin Oncol 21(2): 366-373.
24. Chang J, Couture F, Young S, McWatters KL, Lau CY (2005) Weekly epoetin alfa maintains hemoglobin, improves quality of life, and reduces transfusion in breast cancer patients receiving chemotherapy. J Clin Oncol 23(12): 2597-2605.
25. Charu V, Belani CP, Gill AN, Bhatt M, Tomita D, Rossi G, Ben-Jacob A (2007) Efficacy and safety of every-2-week darbepoetin alfa in patients with anemia of cancer: A controlled, randomized, open-label phase II trial. Oncologist 12(6): 727-737.
26. Christodoulou C, Dafni U, Aravantinos G, Koutras A, Samantas E, Karina M, Janinis J, Papakostas P, Skarlos D, Kalofonos HP, Fountzilas G (2009) Effects of epoetin-alpha on quality of life of cancer patients with solid tumors receiving chemotherapy. Anticancer Res 29(2): 693-702.
27. Cohen J (1988) Statistical Power Analysis for the Behavioral Sciences. 2nd edn. Lawrence Erlbaum: Hillsdale, NJ.
28. CR002305. A Phase III Clinical Trial of PROCRIT (Epoetin Alfa) Versus Placebo in Women Undergoing Adjuvant Chemotherapy for Stage I, II or III Breast Cancer. Study terminated and unpublished (ClinicalTrials.gov Identifier: NCT00246597).
29. Dammacco F, Castoldi G, Rodjer S (2001) Efficacy of epoetin alfa in the treatment of anaemia of multiple myeloma. Br J Haematol 113(1): 172-179.
30. Debus J, Hindermann S, Morr H, Metzger J, Sebastian M, Angermund R, Drings P (2005) Epoetin alfa (EPO) and survival in patients with non-resectable NSCLC-Interim results. Lung Cancer 49(Suppl 3): S57.
31. Demetri GD, Kris M, Wade J, Degos L, Cella D (1998) Quality-of-life benefit in chemotherapy patients treated with epoetin alfa is independent of disease response or tumor type: Results from a prospective community oncology study. Procrit Study Group. J Clin Oncol 16(10): 3412-3425.
32. Duval S (2005) The trim and fill method. Publication Bias in Meta-Analysis-Prevention, Assessment and Adjustments. Wiley: Chichester, pp 127-144.
33. Dwan K, Altman DG, Cresswell L, Blundell M, Gamble CL, Williamson PR (2011) Comparison of protocols and registry entries to published reports for randomised controlled trials. Cochrane Database Syst Rev1: MR000031.
34. Egger M, Smith GD (1998) Bias in location and selection of studies. BMJ 316(7124): 61-66.
35. Eichler HG, Abadie E, Breckenridge A, Leufkens H, Rasi G (2012) Open clinical trial data for all? A view from regulators. PLoS Med 9(4): E1001202.
36. Engert A, Josting A, Haverkamp H, Villalobos M, Lohri A, Sokler M, Zijlstra J, Sturm I, Topp MS, Rank A, Zenz T, Vogelhuber M, Nogova L, Borchmann P, Fuchs M, Flechtner HH, Diehl V (2010) Epoetin alfa in patients with advanced-stage Hodgkin's lymphoma: Results of the randomized placebo-controlled GHSG HD15EPO trial. J Clin Oncol 28(13): 2239-2245.
37. EPO-GER-20. Prospective, randomized, controlled, open phase-IV Study on the treatment of small cell lung cancer (SCLC) in the extensive disease (ED) stage per VALGB Classification with doxorubicin, cyclophosphamide, etoposide (ACE Regimen).
38. Bohlius J, Schmidlin K, Brillant C, Schwarzer G, Trelle S, Seidenfeld J, Zwahlen M, Clarke M, Weingart O, Kluge S, Piper M, Rades D, Steensma DP, Djulbegovic B, Fey MF, Ray-Coquard I, Machtay M, Moebus V, Thomas G, Untch M, Schumacher M, Egger M, Engert A. Recombinant human erythropoiesis-stimulating agents and mortality in patients with cancer: A meta-analysis of randomised trials. Lancet 373(9674): 1532-1542.
39. Fallowfield L, Gagnon D, Zagari M, Cella D, Bresnahan B, Littlewood TJ, McNulty P, Gorzegno G, Freund M. Epoetin Alfa Study Group (2002) Multivariate regression analyses of data from a randomised, double-blind, placebo-controlled study confirm quality of life benefit of epoetin alfa in patients receiving non-platinum chemotherapy. Br J Cancer 87(12): 1341-1353.
40. Fujisaka Y, Sugiyama T, Saito H, Nagase S, Kudoh S, Endo M, Sakai H, Ohashi Y, Saijo N (2011) Randomised, phase III trial of epoetin-beta to treat chemotherapy-induced anaemia according to the EU regulation. Br J Cancer 105(9): 1267-1272.
41. Furukawa TA, Leucht S (2011) How to obtain NNT from Cohen's d: Comparison of two methods. PLoS One 6(4): E19070.
42. Gabrilove JL, Cleeland CS, Livingston RB, Sarokhan B, Winer E, Einhorn LH (2001) Clinical evaluation of once-weekly dosing of epoetin alfa in chemotherapy patients: Improvements in hemoglobin and quality of life are similar to three-times-weekly dosing. J Clin Oncol 19(11): 2875-2882.
43. Glaspy J, Bukowski R, Steinberg D, Taylor C, Tchekmedyian S, Vadhan-Raj S (1997) Impact of therapy with epoetin alfa on clinical outcomes in patients with nonmyeloid malignancies during cancer chemotherapy in community oncology practice. Procrit Study Group. J Clin Oncol 15(3): 1218-1234.
44. Glaspy J, Crawford J, Vansteenkiste J, Henry D, Rao S, Bowers P, Berlin JA, Tomita D, Bridges K, Ludwig H (2010) Erythropoiesis-stimulating agents in oncology: A study-level meta-analysis of survival and other safety outcomes. Br J Cancer 102(2): 301-315.
45. Gordon D, Nichols G, Ben-Jacob A, Tomita D, Lillie T, Miller C (2008) Treating anemia of cancer with every-4-week darbepoetin alfa: Final efficacy and safety results from a phase II, randomized, double-blind, placebo-controlled study. Oncologist 13(6): 715-724.
46. Goss G, Feld R, Bezjak A, Perry G, Melosky B, Smith C, Snee M, Plante R, Lau C (2005) Impact of maintaining Hb with epoetin alfa on time to progression (TTP), overall survival (OS), quality of life (QOL) and transfusion reduction in limited disease SCLC patients. Lung Cancer 49(S53): O-154.
47. Grant MD, Piper M, Bohlius J, Tonia T, Robert N, Vats V, Bonnell C, Ziegler KM, Aronson N (2013) Epoetin and Darbepoetin for Managing Anemia in Patients Undergoing Cancer Treatment: Comparative Effectiveness Update. Agency for Healthcare Research and Quality (US): Rockville, MD, 2013 April Report No.: 13-EHC077-EF. AHRQ Comparative Effectiveness Reviews.
48. Gupta S, Singh PK, Bisth SS, Bhatt ML, Pant M, Gupta R, Singh S, Negi MP (2009) Role of recombinant human erythropoietin in patients of advanced cervical cancer treated 'by chemoradiotherapy'. Cancer Biol Ther 8(1): 13-17.
49. Hedenus M, Adriansson M, San MJ, Kramer MH, Schipperus MR, Juvonen E, Taylor K, Belch A, Altes A, Martinelli G, Watson D, Matcham J, Rossi G, Littlewood TJ (2003) Efficacy and safety of darbepoetin alfa in anaemic patients with lymphoproliferative malignancies: A randomized, doubleblind, placebo-controlled study. Br J Haematol 122(3): 394-403.
50. Henry DH, Abels RI (1994) Recombinant human erythropoietin in the treatment of cancer and chemotherapy-induced anemia: Results of doubleblind and open-label follow-up studies. Semin Oncol 21(2 Suppl 3): 21-28.
51. Hernandez E, Ganly P, Charu V, Dibenedetto J, Tomita D, Lillie T, Taylor K (2009) Randomized, double-blind, placebo-controlled trial of every-3-week darbepoetin alfa 300 micrograms for treatment of chemotherapy-induced anemia. Curr Med Res Opin 25(9): 2109-2120.
52. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414): 557-560.
53. Hoskin PJ, Robinson M, Slevin N, Morgan D, Harrington K, Gaffney C (2009) Effect of epoetin alfa on survival and cancer treatment-related anemia and fatigue in patients receiving radical radiotherapy with curative intent for head and neck cancer. J Clin Oncol 27(34): 5751-5756.
54. Huddart RA, Welch RS, Chan S, Perren T, Atkinson R (2002) A prospective randomised comparative-group evaluation of epoetin alfa for the treatment of anaemia in UK cancer patients receiving platinum-based chemotherapy. [Miscellaneous]. Ann Oncol Abstract Book of the 27th ESMO Congress; Nice, France; 18-22 October.
55. Iconomou G, Koutras A, Rigopoulos A, Vagenakis AG, Kalofonos HP (2003) Effect of recombinant human erythropoietin on quality of life in cancer patients receiving chemotherapy: Results of a randomized, controlled trial. J Pain Symptom Manage 25(6): 512-518.
56. Information for Health Professions. Erythropoiesis-Stimulating Agents (ESA): [Aranesp (darbepoetin), Epogen (epoetin alfa), and Procrit (epoetin alfa)] (2007) http://www.fda.gov/Drugs/DrugSafety/ PostmarketDrugSafetyInformationforPatientsandProviders/ucm126481.htm2007, last accessed: 8 November 2012.
57. INT-1. in: Safety concerns associated with Aranesp (darbepoetin alfa) Amgen, Inc. and Procrit (epoetin alfa) Ortho Biotech, LP, for the treatment of anemia associated with cancer chemotherapy. Department of Health and Human Services, Food and Drug Administration, Center for Drug Evaluation and Research, Oncologic Drugs Advisory Committee.
58. INT-3. in: Safety concerns associated with Aranesp (darbepoetin alfa) Amgen, Inc. and Procrit (epoetin alfa) Ortho Biotech, LP, for the treatment of anemia associated with cancer chemotherapy. Department of Health and Human Services, Food and Drug Administration, Center for Drug Evaluation and Research, Oncologic Drugs Advisory Committee.
59. Kotasek D, Albertsson M, Mackey J. Darbepoetin Alfa 980291 Study Group (2002) Randomized, double-blind, placebocontrolled, dose-finding study of darbepoetin alfa administered once every 3 (Q3W) or 4 (Q4W) weeks in patients with solid tumors. Proc Am Soc Clinical Oncol 21: 356a.
60. Kotasek D, Steger G, Faught W, Underhill C, Poulsen E, Colowick AB, Rossi G, Mackey J (2003) Darbepoetin alfa administered every 3 weeks alleviates anaemia in patients with solid tumours receiving chemotherapy; results of a double-blind, placebo-controlled, randomised study. Eur J Cancer 39(14): 2026-2034.
61. Krzakowski M (2008) Epoetin delta: Efficacy in the treatment of anaemia in cancer patients receiving chemotherapy. Clin Oncol (R Coll Radiol ) 20(9): 705-713.
62. Kumar SM, Zhang G, Bastian BC, Arcasoy MO, Karande P, Pushparajan A, Acs G, Xu X (2012) Erythropoietin receptor contributes to melanoma cell survival in vivo. Oncogene 31(13): 1649-1660.
63. Littlewood TJ, Bajetta E, Nortier JW, Vercammen E, Rapoport B (2001) Effects of epoetin alfa on hematologic parameters and quality of life in cancer patients receiving nonplatinum chemotherapy: Results of a randomized, double-blind, placebo-controlled trial. J Clin Oncol 19(11): 2865-2874.
64. Leyland-Jones B, Semiglazov V, Pawlicki M, Pienkowski T, Tjulandin S, Manikhas G, Makhson A, Roth A, Dodwell D, Baselga J, Biakhov M, Valuckas K, Voznyi E, Liu X, Vercammen E (2005) Maintaining normal hemoglobin levels with epoetin alfa in mainly nonanemic patients with metastatic breast cancer receiving first-line chemotherapy: A survival study. J Clin Oncol 23(25): 5960-5972.
65. Ludwig H, Crawford J, Osterborg A, Vansteenkiste J, Henry DH, Fleishman A, Bridges K, Glaspy JA (2009) Pooled analysis of individual patient-level data from all randomized, double-blind, placebo-controlled trials of darbepoetin alfa in the treatment of patients with chemotherapy-induced anemia. J Clin Oncol 27(17): 2838-2847.
66. Machtay M, Pajak TF, Suntharalingam M, Shenouda G, Hershock D, Stripp DC, Cmelak AJ, Schulsinger A, Fu KK (2007) Radiotherapy with or without erythropoietin for anemic patients with head and neck cancer: A randomized trial of the Radiation Therapy Oncology Group (RTOG 99-03). Int J Radiat Oncol Biol Phys 69(4): 1008-1017.
67. Milroy R, Scagliotti G, van den Berg PM, Galanis NE, Gomez RG, Greil R, Krzakowski M (2003) Early intervention with epoetin alfa maintains hemoglobin (Hb) in advanced non-small cell lung cancer (NSCLC) patients. Lung Cancer 41(Suppl 2): 574.
68. Minton O, Richardson A, Sharpe M, Hotopf M, Stone P (2008) A systematic review and meta-analysis of the pharmacological treatment of cancer-related fatigue. J Natl Cancer Inst 20 100(16): 1155-1166.
69. Minton O, Richardson A, Sharpe M, Hotopf M, Stone P (2010) Drug therapy for the management of cancer-related fatigue. Cochrane Database Syst Rev 7: CD006704.
70. Moebus V, Jackisch C, Schneeweiss A, Huober J, Lueck HJ, du Bois A, Thomssen C, Kurbacher C, Kuhn W, Nitz U, Runnebaum IB, Hinke A, Kreienberg R, Untch M (2013) AGO Breast Study Group. Adding epoetin alfa to intense dose-dense adjuvant chemotherapy for breast cancer: Randomized clinical trial. J Natl Cancer Inst 105(14): 1018-1026.
71. Moher D, Liberati A, Tetzlaff J, Altman DG, the PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med 6(6): E1000097.
72. Mystakidou K, Kalaidopoulou O, Katsouda E, Parpa E, Kouskouni E, Chondros C, Tsiatas ML, Vlahos L (2005) Evaluation of epoetin supplemented with oral iron in patients with solid malignancies and chronic anemia not receiving anticancer treatment. Anticancer Res 25(5): 3495-3500.
73. Nitz U, Gluz O, Oberhoff C, Reimer T, Schumacher C, Hackmann J, Warm M, Uleer C, Runde V, Kuemmel S, Zuna I, Harbeck N (2011) Adjuvant chemotherapy with or without Darbepoetin alpha in node-positive breast cancer: Survival and Quality of Life analysis from the prospective randomized WSG ARA Plua Trial. Cancer Res 71(Suppl 24): PD07-06.
74. O'Shaughnessy JA, Vukelja SJ, Holmes FA, Savin M, Jones M, Royall D, George M, Von HD (2005) Feasibility of quantifying the effects of epoetin alfa therapy on cognitive function in women with breast cancer undergoing adjuvant or neoadjuvant chemotherapy. Clin Breast Cancer 5(6): 439-446.
75. OBE/EPO-INT-03. A randomised comparison of the effect of maintaining haemoglobin levels with weekly epoetin alfa or with conventional anaemia management in subjects with Multiple Myeloma undergoing chemotherapy (EMMY); Protocol No: OBE/EPO-INT-03. Cited in Bohlius J, Schmidlin K, Brillant C, Schwarzer G, Trelle S, Seidenfeld J, Zwahlen M, Clarke M, Weingart O, Kluge S, Piper M, Rades D, Steensma DP, Djulbegovic B, Fey MF, Ray-Coquard I, Machtay M, Moebus V, Thomas G, Untch M, Schumacher M, Egger M, Engert A. Recombinant human erythropoiesis-stimulating agents and mortality in patients with cancer: A meta-analysis of randomised trials. Lancet 373(9674): 1532-1542.
76. Osterborg A, Brandberg Y, Molostova V, Iosava G, Abdulkadyrov K, Hedenus M, Messinger D (2002) Randomized, double-blind, placebo-controlled trial of recombinant human erythropoietin, epoetin Beta, in hematologic malignancies. J Clin Oncol 20(10): 2486-2494.
77. P-174 in: Safety concerns associated with Aranesp (darbepoetin alfa) Amgen, Inc. and Procrit (epoetin alfa) Ortho Biotech, LP, for the treatment of anemia associated with cancer chemotherapy. Department of Health and Human Services, Food and Drug Administration, Center for Drug Evaluation and Research, Oncologic Drugs Advisory Committee.
78. Pirker R, Ramlau RA, Schuette W, Zatloukal P, Ferreira I, Lillie T, Vansteenkiste JF (2008) Safety and efficacy of darbepoetin alpha in previously untreated extensive-stage small-cell lung cancer treated with platinum plus etoposide. J Clin Oncol 26(14): 2342-2349.
79. Pronzato P, Cortesi E, van der Rijt CC, Bols A, Moreno-Nogueira JA, de Oliveira CF, Barrett-Lee P, Ostler PJ, Rosso R (2010) Epoetin alfa improves anemia and anemia-related, patient-reported outcomes in patients with breast cancer receiving myelotoxic chemotherapy: Results of a European, multicenter, randomized, controlled trial. Oncologist 15(9): 935-943.
80. Quirt I, Robeson C, Lau CY, Kovacs M, Burdette-Radoux S, Dolan S, Tang SC, McKenzie M, Couture F (2001) Epoetin alfa therapy increases hemoglobin levels and improves quality of life in patients with cancer-related anemia who are not receiving chemotherapy and patients with anemia who are receiving chemotherapy. J Clin Oncol 19(21): 4126-4134.
81. Ray-Coquard I, Dussart S, Goillot C, Mayeur D, Debourdeau P, Ghesquieres H, Bachelot T, Le CA, Anglaret B, Agostini C, Guastalla JP, Lancry L, Biron P, Desseigne F, Blay JY (2009) A risk model for severe anemia to select cancer patients for primary prophylaxis with epoetin alpha: A prospective randomized controlled trial of the ELYPSE study group. Ann Oncol 20(6): 1105-1112.
82. Redmond S, von Elm E, Blümle A, Gengler M, Gsponer T, Egger M (2013) Cohort study of trials submitted to ethics committee identified discrepant reporting of outcomes in publications. J Clin Epidemiol 66(12): 1367-1375.
83. Reichenbach S, Sterchi R, Scherer M, Trelle S, Burgi E, Burgi U, Dieppe PA, Juni P (2007) Meta-analysis: Chondroitin for osteoarthritis of the knee or hip. Ann Intern Med 146(8): 580-590.
84. Rizzo JD, Brouwers M, Hurley P, Seidenfeld J, Arcasoy MO, Spivak JL, Bennett CL, Bohlius J, Evanchuk D, Goode MJ, Jakubowski AA, Regan DH, Somerfield MR (2010) American Society of Clinical Oncology/American Society of Hematology clinical practice guideline update on the use of epoetin and darbepoetin in adult patients with cancer. J Clin Oncol 28(33): 4996-5010.
85. Rose E, Rai K, Revicki D, Brown R, Reblando J and the EPO in Anemia of CLL Study Group (1994) Clinical and health status assessments in anemic chronic lymphocytic leukemia (CLL) patients treated with epoetin alfa (EPO). Blood 84(10 Suppl 1): 526a.
86. Savonije JH, van Groeningen CJ, van BA, Honkoop AH, van Felius CL, Wormhoudt LW, Giaccone G (2005) Effects of early intervention with epoetin alfa on transfusion requirement, hemoglobin level and survival during platinum-based chemotherapy: Results of a multicenter randomised controlled trial. Eur J Cancer 41(11): 1560-1569.
87. Schrijvers D, De SH, Roila F (2010) Erythropoiesis-stimulating agents in the treatment of anaemia in cancer patients: ESMO Clinical Practice Guidelines for use. Ann Oncol 21(Suppl 5): V244-v247.
88. Seidenfeld J, Piper M, Bohlius J, Weingart O, Trelle S, Engert A, Skoetz N, Schwarzer G, Wilson J, Brunskill S, Hyde C, Bonnell C, Ziegler KM, Aronson N (2006) Comparative Effectiveness of Epoetin and Darbepoetin for Managing Anemia in Patients Undergoing Cancer Treatment [Internet]. Rockville (MD): Agency for Healthcare Research and Quality (US); AHRQ Comparative Effectiveness Reviews.
89. Sloan JA, Dueck A (2004) Issues for statisticians in conducting analyses and translating results for quality of life end points in clinical trials. J Biopharm Stat 14(1): 73-96.
90. Sloan JA, Frost MH, Berzon R, Dueck A, Guyatt G, Moinpour C, Sprangers M, Ferrans C, Cella D (2006) The clinical significance of quality of life assessments in oncology: A summary for clinicians. Support Care Cancer 14(10): 988-998.
91. Smith Jr RE, Aapro MS, Ludwig H, Pinter T, Smakal M, Ciuleanu TE, Chen L, Lillie T, Glaspy JA (2008) Darbepoetin alpha for the treatment of anemia in patients with active cancer not receiving chemotherapy or radiotherapy: Results of a phase III, multicenter, randomized, double-blind, placebocontrolled study. J Clin Oncol 26(7): 1040-1050.
92. Sterne JA, Egger M (2001) Funnel plots for detecting bias in meta-analysis: Guidelines on choice of axis. J Clin Epidemiol 54(10): 1046-1055.
93. Strauss HG, Haensgen G, Dunst J, Hayward CR, Burger HU, Scherhag A, Koelbl H (2008) Effects of anemia correction with epoetin beta in patients receiving radiochemotherapy for advanced cervical cancer. Int J Gynecol Cancer 18(3): 515-524.
94. Suzuki Y, Tokuda Y, Okamoto R, Nakagawa K, Ando K, Iwata H, Tobinai K, Tanigawara Y, Hotta T, Saijo N (2008) Randomized, placebo-controlled phase II study of darbepoetin alfa (DA) administered every three weeks (Q3W) in patients with chemotherapy induced anemia (CIA). Ann Oncol 19(Suppl 8): 8277.
95. Szenajch J, Wcislo G, Jeong JY, Szczylik C, Feldman L (2010) The role of erythropoietin and its receptor in growth, survival and therapeutic response of human tumor cells From clinic to bench-a critical review. Biochim Biophys Acta 1806(1): 82-95.
96. Thatcher N, De Campos ES, Bell DR, Steward WP, Varghese G, Morant R, Vansteenkiste JF, Rosso R, Ewers SB, Sundal E, Schatzmann E, Stocker H (1999) Epoetin alpha prevents anaemia and reduces transfusion requirements in patients undergoing primarily platinum-based chemotherapy for small cell lung cancer. Br J Cancer 80(3-4): 396-402.
97. Thomas G, Ali S, Hoebers FJ, Darcy KM, Rodgers WH, Patel M, Abulafia O, Lucci III JA, Begg AC (2008) Phase III trial to evaluate the efficacy of maintaining hemoglobin levels above 12.0 g/dl with erythropoietin vs above 10.0 g/dl without erythropoietin in anemic patients receiving concurrent radiation and cisplatin for cervical cancer. Gynecol Oncol 108(2): 317-325.
98. Thomas H, McAdam KF, Thomas RJ, Joffe JK, Sugden EM, Awwad ST, Tan LT, Murray PA, Bailey N, Branson AN (2002) Early intervention with epoetin alfa for treatment of anaemia and improvement of quality of life in cancer patients undergoing myelotoxic chemotherapy. Ann Oncol 13(Suppl 5): 177.
99. Thompson SG, Sharp SJ (1999) Explaining heterogeneity in meta-analysis: A comparison of methods. Stat Med 18(20): 2693-2708.
100. Tonelli M, Hemmelgarn B, Reiman T, Manns B, Reaume MN, Lloyd A, Wiebe N, Klarenbach S (2009) Benefits and harms of erythropoiesisstimulating agents for anemia related to cancer: A meta-analysis. CMAJ 180(11): E62-E71.
101. Tonia T, Mettler A, Robert N, Schwarzer G, Seidenfeld J, Weingart O, Hyde C, Engert A, Bohlius J (2012) Erythropoietin or darbepoetin for patients with cancer. Cochrane Database Syst Rev 12: CD003407.
102. Tsuboi M, Ezaki K, Tobinai K, Ohashi Y, Saijo N (2009) Weekly administration of epoetin beta for chemotherapy-induced anemia in cancer patients: Results of a multicenter, Phase III, randomized, double-blind, placebo-controlled study. Jpn J Clin Oncol 39(3): 163-168.
103. Untch M, von Minckwitz G, Konecny GE, Conrad U, Fett W, Kurzeder C, Lück HJ, Stickeler E, Urbaczyk H, Liedtke B, Beckmann MW, Salat C, Harbeck N, Müller V, Schmidt M, Hasmüller S, Lenhard M, Nekljudova V, Lebeau A, Loibl S, Fasching PA. Arbeitsgemeinschaft Gynäkologische Onkologie PREPARE investigators (2011) PREPARE trial: A randomized phase III trial comparing preoperative, dose-dense, dose-intensified chemotherapy with epirubicin, paclitaxel, and CMF versus a standarddosed epirubicin- cyclophosphamide followed by paclitaxel with or without darbepoetin alfa in primary breast cancer-outcome on prognosis. Ann Oncol 22(9): 1999-2006.
104. Vansteenkiste J, Pirker R, Massuti B, Barata F, Font A, Fiegl M, Siena S, Gateley J, Tomita D, Colowick AB, Musil J (2002) Double-blind, placebo-controlled, randomized phase III trial of darbepoetin alfa in lung cancer patients receiving chemotherapy. J Natl Cancer Inst 94(16): 1211-1220.
105. Ware Jr JE, Sherbourne CD (1992) The MOS 36-item short-form health survey (SF-36). I. Conceptual framework and item selection. Med Care 30(6): 473-483.
106. Wilkinson PM, Antonopoulos M, Lahousen M, Lind M, Kosmidis P (2006) Epoetin alfa in platinum-treated ovarian cancer patients: Results of a multinational, multicentre, randomised trial. Br J Cancer 94(7): 947-954.
107. Winquist E, Julian JA, Moore MJ, Nabid A, Sathya J, Wood L, Venner P, Levine M (2009) Randomized, double-blind, placebo-controlled trial of epoetin alfa in men with castration-resistant prostate cancer and anemia. J Clin Oncol 27(4): 644-646.
108. Witzig TE, Silberstein PT, Loprinzi CL, Sloan JA, Novotny PJ, Mailliard JA, Rowland KM, Alberts SR, Krook JE, Levitt R, Morton RF (2005) Phase III, randomized, double-blind study of epoetin alfa compared with placebo in anemic patients receiving chemotherapy. J Clin Oncol 23(12): 2606-2617.
109. Wright JR, Ung YC, Julian JA, Pritchard KI, Whelan TJ, Smith C, Szechtman B, Roa W, Mulroy L, Rudinskas L, Gagnon B, Okawara GS, Levine MN (2007) Randomized, double-blind, placebo-controlled trial of erythropoietin in non-small-cell lung cancer with disease-related anemia. J Clin Oncol 25(9): 1027-1032.
110. Yellen SB, Cella DF, Webster K, Blendowski C, Kaplan E (1997) Measuring fatigue and other anemia-related symptoms with the Functional Assessment of Cancer Therapy (FACT) measurement system. J Pain Symptom Manage 13(2): 63-74.
111. Yoshizaki A, Kumagai S, Sugiyama T, Goto I, Saito H, Ariyoshi Y, Saijo N, Ohashi Y (2010) A phase III, randomized double-blind placebo controlled study of epoetin beta in luing and gynecological cancer receiving platinum-based chemotherapy: Japan Erythropoietin study group. Ann Oncol 21(Suppl8): Viii385.